Influence of climatic factors on spatio-temporal variabilities in the occurrence of aflatoxins in major food grains available at retail shops in Bangladesh
DOI:
https://doi.org/10.3329/aajfss.v8i2.72825Keywords:
food grains, aflatoxins, seasonlity, climatic factorsAbstract
In Bangladesh, little is known about the role of climatic factors influencing spatio-temporal occurrence among different food grains of aflatoxins, which have been linked to liver cancer cases and other health hazards. In this study, 252 food grain samples of 10 types were collected from retail markets at 18 districts, pre-monsoon, monsoon and post-monsoon seasons during February-September, 2018. Occurrence and concentration of total aflatoxins in the samples were analysed by a direct competitive enzyme-linked immunosorbent assay, and compared with climatic data (temperature, humidity, rainfall, and sunshine hours). Contamination of aflatoxins was found in approx. 38% (n=96) of the total samples, with highest occurrence in groundnuts (82%), followed by corn grains (70%), chick pea (54.5%), wheat grain (50%) and green gram (42.9%). Aflatoxins occurrence was moderate in split chick pea (30.8%), yellow pea (28.2%), black gram (27.8%), and lentils (27.6%), while the lowest in grass pea (17.6%). Aflatoxins concentration was found to exceed the European Union permissible limit (≤5 µg kg-1) in 33 (13.1%) samples. Overall, approximately 5.6%, 7.5%, and 25.0% samples were contaminated with high (10-19 ppb), medium (5-9 ppb) and low (1-4 ppb) concentrations of aflatoxins, respectively. High level concentration of aflatoxins was more frequent in groundnut (36%) and wheat grain (20%), in comparison to other types. Occurrence of aflatoxins during pre-monsoon was detected among 21% (19/91) samples, which increased to ca. 30% (36/119) during monsoon, and 98% (41/42) during post-monsoon. However, aflatoxins mean concentration during post-monsoon was comparatively low than the other seasons. Variations in aflatoxins monthly prevalence correlated significantly with relative humidity (p ≤ 0.01) and rainfall (p≤ 0.05), when a 1-month time lag was considered. Therefore, predisposing climatic conditions, i.e., rainfall incidences and persistence of higher relative humidity in the previous month(s), have salient influence on aflatoxins occurrence, potentially impacting both pre-harvest and stored food grains. This study underscores the need of a more holistic monitoring of aflatoxins in agricultural products for a longer term, and adoption of proper intervention measures for food grains while being stored and before consumption.
Asian Australas. J. Food Saf. Secur. 2024, 8(2), 32-47
Downloads
205
118
References
Acuña‐Gutiérrez C, VM Jiménez and J Müller, 2022. Occurrence of mycotoxins in pulses. Comp. Rev. Food Sci. Food Safe., 21: 4002-4017.
Ali N, K Hossain, M Blaszkewicz, M Rahman, NC Mohanto, A Alim and GH Degen, 2016. Occurrence of aflatoxin M1 in urines from rural and urban adult cohorts in Bangladesh. Arch. Toxicol., 90, 1749-1755.
Bauchet J, S Prieto and J Ricker-Gilbert, 2021. Improved drying and storage practices that reduce aflatoxins in stored maize: experimental evidence from smallholders in Senegal. Am. J. Agric. Econ., 103: 296-316.
Bediako KA, K Ofori, SK Offei, D Dzidzienyo, JY Asibuo and RA Amoah, 2019. Aflatoxin contamination of groundnut (Arachis hypogaea L.): Predisposing factors and management interventions. Food Cont., 98: 61-67.
Bennett JW, S Kale and J Yu, 2007. Aflatoxins: background, toxicology, and molecular biology. Foodborne Dis., 355-373.
Bhatnagar-Mathur P, S Sunkara, M Bhatnagar-Panwar, F Waliyar and KK Sharma, 2015. Biotechnological advances for combating Aspergillus flavus and aflatoxin contamination in crops. Plant Sci., 234:119-132.
Bhuiyan MNH, MT Hassan, M Begum, M Ahan and M Rahim, 2013. Occurrence and seasonal trends of aflatoxin in rice, maize and wheat in Bangladesh. Int. J. Sustain. Agril. Tech., 9: 8-14.
Chen YC, CD Liao, HY Lin, LC Chiueh and DYC Shih, 2013. Survey of aflatoxin contamination in peanut products in Taiwan from 1997 to 2011. J. Food Drug Anal., 21: 247-252.
Cotty PJ and R Jaime-Garcia, 2007. Influences of climate on aflatoxin producing fungi and aflatoxin contamination. Int. J. Food Microbiol., 119: 109-115.
Damianidis D, BV Ortiz, KL Bowen, GL Windham, G Hoogenboom, A Hagan and S Mourtzinis, 2018. Minimum temperature, rainfall, and agronomic management impacts on corn grain aflatoxin contamination. Agron. J., 110: 1697-1708.
Dawlatana M, RD Coker, MJ Nagler, CP Wild, MS Hassan and G Blunden, 2002. The occurrence of mycotoxins in key commodities in Bangladesh: surveillance results from 1993 to 1995. J. Nat. Tox., 11: 379-386.
Ding N, F Xing, X Liu, JN Selvaraj, L Wang, Y Zhao and Y Liu, 2015. Variation in fungal microbiome (mycobiome) and aflatoxin in stored in-shell peanuts at four different areas of China. Front. Microbial., 6: 1055.
EC, 2010. European Commission. Commission Regulation (EC) No 165/2010 of 26 February 2010 amending Regulation (EC) No 1881/2006 setting maximum levels for certain contaminants in foodstuffs as regards aflatoxins. Off. J. Eur. Union L, 50: 8–12.
Firdous S, A Ashfaq, SJ Khan and N Khan, 2014. Aflatoxins in corn and rice sold in Lahore, Pakistan. Food Add. Cont. Part B, 7: 95-98.
Galván AI, A Rodríguez, A Martín, MJ Serradilla, A Martínez-Dorado and MDG Córdoba, 2021. Effect of temperature during drying and storage of dried figs on growth, gene expression and aflatoxin production. Toxins, 13: 134.
Giorni P, T Bertuzzi and P Battilani, 2016. Aflatoxin in maize, a multifaceted answer of Aspergillus flavus governed by weather, host-plant and competitor fungi. J. Cer. Sci., 70: 256-262.
Huang C, A Jha, R Sweany, C DeRobertis and JKE Damann, 2011. Intraspecific aflatoxin inhibition in Aspergillus flavus is thigmoregulated, independent of vegetative compatibility group and is strain dependent. PLoS One, 6: e23470.
Iqbal SZ, MR Asi, M Zuber, N Akram and N Batool, 2013. Aflatoxins contamination in peanut and peanut products commercially available in retail markets of Punjab, Pakistan. Food Cont., 32: 83-86.
Jaibangyang S, R Nasanit and S Limtong, 2020. Biological control of aflatoxin-producing Aspergillus flavus by volatile organic compound-producing antagonistic yeasts. BioControl, 65: 377-386.
Jannat M, Masud MM, M Nusrat, S Bashar, MM Mita, MI Hossain and MR Islam, 2022. Aflatoxins and fumonisins contamination of maize in Bangladesh: an emerging threat for safe food and food security. Maize Genetic Resources: Breeding Strategies and Recent Advances, 69: 101647.
Johnsson P, M Lindblad, A Thim, N Jonsson, E Vargas, N Medeiros and M Olsen, 2008. Growth of aflatoxigenic moulds and aflatoxin formation in Brazil nuts. World Mycot. J., 1: 127-137.
Khan MMH, B Chowdhury, MR Bhuiya and M Rahim, 2005. Variation of aflatoxin level in different poultry feeds used in different poultry farms of Bangladesh round the year. Int. J. Poult. Sci., 4: 382-387.
Khandaker M, R Ahmed, M Rahim, T Hassan and M Begum, 2019. Determination of mycoflora and mycotoxins in raw and roasted peanuts in Bangladesh. Int. J. Plant Environ., 5: 259-264.
Khlangwiset P, GS Shephard and F Wu, 2011. Aflatoxins and growth impairment: a review. Crit. Rev. Toxicol., 41: 740-755.
Klich MA, 2007. Aspergillus flavus: the major producer of aflatoxin. Mole. Plant Pathol., 8: 713-722.
Koirala P, S Kumar, BK Yadav and KC Premarajan, 2005. Occurrence of aflatoxin in some of the food and feed in Nepal. Indian J. Med. Sci., 59: 331-336.
Kumar A, H Pathak, S Bhadauria and J Sudan, 2021. Aflatoxin contamination in food crops: causes, detection, and management: a review. Food Prod. Proc. Nutri., 3:1-9.
Kyei NN, B Cramer, HU Humpf, GH Degen, N Ali and S Gabrysch, 2022. Assessment of multiple mycotoxin exposure and its association with food consumption: a human biomonitoring study in a pregnant cohort in rural Bangladesh. Arch. Toxicol., 96: 2123-2138.
Lahouar A, S Marin, A Crespo-Sempere, S Saïd and V Sanchis, 2016. Effects of temperature, water activity and incubation time on fungal growth and aflatoxin B1 production by toxinogenic Aspergillus flavus isolates on sorghum seeds. Rev. Argentina Microbiol., 48: 78-85.
Leszczyńska J, J Masłowska, A Owczarek and U Kucharska, 2001. Determination of aflatoxins in food products by the ELISA method. Czech J. Food Sci., 19: 8-12.
Lubna MA, M Debnath and F Hossaini, 2018. Detection of aflatoxin in poultry feed and feed materials through immuno based assay from different poultry farms and feed factories in Bangladesh. Bangladesh J. Microbiol., 35: 75-78.
Mahato DK, KE Lee, M Kamle, S Devi, KN Dewangan, P Kumar and SG Kang, 2019. Aflatoxins in food and feed: an overview on prevalence, detection and control strategies. Front. Microbiol., 10: 2266.
Mahfuz M, MA Alam, SM Fahim, MA Gazi, MJ Raihan, M Hossain and T Ahmed, 2019. Aflatoxin exposure in children living in Mirpur, Dhaka: data from MAL-ED companion study. J. Expo. Sci. Environ. Epidemiol., 29: 655-662.
Mannaa M and KD Kim, 2017. Influence of temperature and water activity on deleterious fungi and mycotoxin production during grain storage. Mycobiology, 45: 240-254.
Marchese S, A Polo, A Ariano, S Velotto, S Costantini and L Severino, 2018. Aflatoxin B1 and M1: Biological properties and their involvement in cancer development. Toxins, 10: 214.
Matumba L, L Singano, L Pungulani, N Mvula, A Matumba, C Singano and G Matita, 2017. Aflatoxins, discolouration and insect damage in dried cowpea and pigeon pea in Malawi and the effectiveness of flotation/washing operation in eliminating the aflatoxins. Mycot. Res., 33: 129-137.
Milani J and G Maleki, 2014. Effects of processing on mycotoxin stability in cereals. J. Sci. Food Agric., 94: 2372-2375.
Monyo ES, SMC Njoroge, R Coe, M Osiru, F Madinda, F Waliyar and S Anitha, 2012. Occurrence and distribution of aflatoxin contamination in groundnuts (Arachis hypogaea L) and population density of Aflatoxigenic Aspergilli in Malawi. Crop Prote., 42: 149-155.
Nazir A, I Kalim, M Sajjad, M Usman and M Iqbal, 2019. Prevalence of aflatoxin contamination in pulses and spices in different regions of Punjab. Chem. Int, 5: 274.
Negash D, 2018. A review of aflatoxin: occurrence, prevention, and gaps in both food and feed safety. J. App. Microbiol. Res., 1: 35-43.
Norlia M, S Jinap, MAR Nor-Khaizura, S Radu, NIP Samsudin and FA Azri, 2019. Aspergillus section Flavi and aflatoxins: Occurrence, detection, and identification in raw peanuts and peanut-based products along the supply chain. Front. Microbiol., 10: 2602.
Obonyo MA and EN Salano, 2018. Perennial and seasonal contamination of maize by aflatoxins in eastern Kenya. Int. J. Food Contamin., 5: 1-5.
Ok HE, HJ Kim, WB Shim, H Lee, DH Bae, DH Chung and HS Chun, 2007. Natural occurrence of aflatoxin B1 in marketed foods and risk estimates of dietary exposure in Koreans. J. Food Prot., 70: 2824-2828.
Okoth S, M De Boevre, A Vidal, DMJ Diana, S Landschoot, M Kyallo and S De Saeger, 2018. Genetic and toxigenic variability within Aspergillus flavus population isolated from maize in two diverse environments in Kenya. Front. Microbiol., 9: 57.
Ostry V, F Malir, J Toman and Y Grosse, 2017. Mycotoxins as human carcinogens—the IARC Monographs classification. Mycot. Res., 33: 65-73.
Pandey I and SS Chauhan, 2007. Studies on production performance and toxin residues in tissues and eggs of layer chickens fed on diets with various concentrations of aflatoxin AFB1. British Poult. Sci., 48: 713-723.
Pratiwi C, WP Rahayu, HN Lioe, D Herawati, W Broto and S Ambarwati, 2015. The effect of temperature and relative humidity for Aspergillus flavus BIO 2237 growth and aflatoxin production on soybeans. Int. Food Res. J., 22: 82-87
Rastegar H, S Shoeibi, H Yazdanpanah, M Amirahmadi, AM Khaneghah, FB Campagnollo and AS Sant’Ana, 2017. Removal of aflatoxin B1 by roasting with lemon juice and/or citric acid in contaminated pistachio nuts. Food Cont., 71: 279-284.
Richard JL, 2007. Some major mycotoxins and their mycotoxicoses—An overview. Int. J. Food Microbial., 119: 3-10.
Rafik M, F Afroz and MM Rahman, 2020. Detection of aflatoxin-producing fungi in maize. Bangladesh Vet., 37: 27-35.
Roy M, J Harris, S Afreen, E Deak, L Gade, SA Balajee and S Luby, 2013. Aflatoxin contamination in food commodities in Bangladesh. Food Add. Cont. Part B, 6: 17-23.
Sanchis V and N Magan, 2004. Environmental conditions affecting mycotoxins. Mycotoxins Food Detec. Cont., 1: 174-189.
Schmidt-Heydt M, CE Rüfer, A Abdel-Hadi, N Magan and R Geisen, 2010. The production of aflatoxin B1 or G1 by Aspergillus parasiticus at various combinations of temperature and water activity is related to the ratio of aflS to aflR expression. Mycot. Res., 26: 241-246.
Smith LE, M Stasiewicz, R Hestrin, L Morales, S Mutiga and RJ Nelson, 2016. Examining environmental drivers of spatial variability in aflatoxin accumulation in Kenyan maize: Potential utility in risk prediction models. African J. Food, Agric. Nut. Dev., 16: 11086-11105.
Stasiewicz MJ, TD Falade, M Mutuma, SK Mutiga, JJ Harvey, G Fox and RJ Nelson, 2017. Multi-spectral kernel sorting to reduce aflatoxins and fumonisins in Kenyan maize. Food Cont., 78: 203-214.
Sultana A, M Shoeb, MIR Mamun and N Nahar, 2021. Analysis of aflatoxins; B1, B2, G1, and G2 in some rice samples of Bangladesh. J. Bangladesh Acad. Sci., 45: 187-196.
Taheri N, S Semnani, G Roshandel, M Namjoo, H Keshavarzian, AG Chogan and H Joshaghani, 2012. Aflatoxin contamination in wheat flour samples from Golestan Province, Northeast of Iran. Iranian journal of public health, 41: 42.
Temba BA, RE Darnell, A Gichangi, D Lwezaura, PG Pardey, JJ Harvey and DJ Kriticos 2021. The influence of weather on the occurrence of aflatoxin b1 in harvested maize from Kenya and Tanzania. Foods, 10: 216.
Torres AM, GG Barros, SA Palacios, SN Chulze and P Battilani, 2014. Review on pre-and post-harvest management of peanuts to minimize aflatoxin contamination. Food Res. Int., 62: 11-19.
Toteja GS, A Mukherjee, S Diwakar, P Singh, BN Saxena, KK Sinha and S Parkar, 2006. Aflatoxin B1 contamination in wheat grain samples collected from different geographical regions of India: a multicenter study. J. Food Prot., 69: 1463-1467.
Turna NS and F Wu, 2021. Aflatoxin M1 in milk: A global occurrence, intake, and exposure assessment. Tren. Food Sci. Technol., 110: 183-192.
Ubwa ST, J Abah, BO Atu, RL Tyohemba and JT Yande, 2014. Assessment of total aflatoxins level of two major nuts consumed in Makurdi Benue State, Nigeria. Int. J. Nutri. Food Sci., 3: 397-403.
Van den Besselaar EJ, A Sanchez‐Lorenzo, M Wild, AM Klein Tank and ATJ De Laat, 2015. Relationship between sunshine duration and temperature trends across Europe since the second half of the twentieth century. J. Geophy. Res. Atmos., 120: 10-823.
Wacoo AP, D Wendiro, PC Vuzi and JF Hawumba, 2014. Methods for detection of aflatoxins in agricultural food crops. J. App. Chem., 2014: 706291.
Waliyar F, M Osiru, BR Ntare, KVK Kumar, H Sudini, A Traore and B Diarra, 2015a. Post-harvest management of aflatoxin contamination in groundnut. World Mycot. J., 8: 245-252.
Waliyar F, VC Umeh, A Traore, M Osiru, BR Ntare, B Diarra and H Sudini, 2015b. Prevalence and distribution of aflatoxin contamination in groundnut (Arachis hypogaea L.) in Mali, West Africa. Crop Prot., 70: 1-7.
Wu F, JD Groopman and JJ Pestka, 2014. Public health impacts of foodborne mycotoxins. Ann. Rev. Food Sci. Technol., 5: 351-372.
Yazdanpanah H, T Mohammadi, G Abouhossain and AM Cheraghali, 2005. Effect of roasting on degradation of aflatoxins in contaminated pistachio nuts. Food Chem. Toxicol., 43: 1135-1139.
Zain ME, 2011. Impact of mycotoxins on humans and animals. J. Saudi Chem. Soc., 15: 129-144.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Sucharit Basu Neogi, Md Nasir Uddin, Mohammad Arif, Ashis Ratan Sen, Priyanka Rani Paul, Md Jahidul Islam Saddam, AKM Ziaul Haque, Seksun Samosornsuk, Worada Samosornsuk, SM Lutful Kabir
This work is licensed under a Creative Commons Attribution 4.0 International License.